Directory UMM :Data Elmu:jurnal:A:Applied Animal Behaviour Science:Vol69.Issue4.Oct2000:
Applied Animal Behaviour Science 69 Ž2000. 255–264
www.elsevier.comrlocaterapplanim
Thwarting of behaviour in different contexts and the
gakel-call in the laying hen
Patrick H. Zimmerman a,) , Paul Koene a , Jan A.R.A.M. van Hooff
a
b
Ethology Group, Wageningen Agricultural UniÕersity, P.O. Box 338, 6700 AH Wageningen, Netherlands
b
Project Group Ethology and Socio-Ecology, P.O. Box 80086, 3508 TB Utrecht, Netherlands
Accepted 14 April 2000
Abstract
Earlier studies have shown that thwarting of feeding behaviour in the laying hen is expressed
through a specific vocalisation, the gakel-call. The first aim of this study was to investigate
whether the effect of deprivation per se on the occurrence of gakel-calls can be distinguished from
the effect of the additional frustration. Frustration is defined as the state of an animal that results
from nonreward in the expectancy of reward. The second aim was to investigate whether the
occurrence of gakel-calls is restricted to a food context or whether it can be regarded as an
expression of frustration in general. For this purpose, 20 hens were deprived of food, water and
dustbath. After deprivation at a fixed time, a cue was given and the hens were rewarded with
access to food, water or dust during a 15-min session on 4 consecutive days. On the fifth day, they
were thwarted in the associated behaviours by blocking the access to these commodities, after the
hens had been presented the signal that previously preceded the reward. We then recorded
behaviours that might reflect the state of frustration in three 15-min periods. The period
‘‘Pre-Frustration’’ started 15 min before ‘‘Frustration’’. This, in turn, was followed by the period
‘‘Post-frustration’’ in which the hens were rewarded again. Nesting behaviour was thwarted by
blocking the access to the nest ŽFrustration. after a hen had reached the last stage of its prelaying
behaviour.
In the food, water and dustbath context, deprivation elicited gakel-calls. The additional
frustration resulted in a higher number of gakel-calls in all contexts except the food context.
However, together with the findings of previous experiments, the results of this study suggest that
frustration, in general, is expressed through the gakel-call. Frustration in the nest context elicited
more gakel-calls than the other contexts. This latter finding is discussed in the light of the
)
Corresponding author. Tel.: q31-317-483926; fax: q31-317-485006.
E-mail address: patrick.zimmerman@etho.vh.wau.nl ŽP.H. Zimmerman..
0168-1591r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 1 5 9 1 Ž 0 0 . 0 0 1 3 7 - 4
256
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
occurrence of the gakel-call under natural circumstances. q 2000 Elsevier Science B.V. All rights
reserved.
Keywords: Chicken welfare; Frustration; Deprivation; Vocalisation; Feeding; Drinking; Dustbathing; Prelaying
1. Introduction
In domestic laying hens, an increase in behaviours such as stereotyped pacing,
displacement preening and the occurrence of a specific vocalisation, the gakel-call, is
associated with thwarting of feeding ŽDuncan and Wood-Gush, 1972a,b; Schenk et al.,
1983; Zimmerman and Koene, 1998a., dustbathing ŽKoene and Wiepkema, 1991. and
nesting behaviour Že.g. Schenk et al., 1983; Meijsser and Hughes, 1989; Freire et al.,
1996.. Thwarting a behaviour that ensures fulfillment of ethological needs impairs
welfare. Animal welfare is the state of the animal regarding its attempt to fulfill its needs
ŽBroom, 1996.. A number of studies suggests that the gakel-call is given in reaction to
the thwarting of behaviour ŽSchenk et al., 1983; Meijsser and Hughes, 1989; Koene and
Wiepkema, 1991; Zimmerman and Koene, 1998a.. Behaviours, which are given in
response to the thwarting of behaviour, can be used as indicators of the subsequent state
of frustration and may, therefore, qualify as measures of welfare ŽDawkins, 1990;
Duncan, 1992.. Frustration has been defined as ‘‘an aversive motivational state that
results from nonreward, reduced reward or delayed reward in the presence of a history
of reward’’ ŽAmsel, 1992.. From this definition, it follows that the effect of mere
thwarting of behaviour might be distinguishable from the effect of frustration. The first
aim of the present study was to investigate whether the effect of deprivation on the
occurrence of gakel-calls could be distinguished from the effect of the additional
frustration.
Under natural conditions, it has been described that a female hen, which is about to
leave the group to find a suitable nest site, utters the gakel-call. As a rule, the dominant
male responds to the gakel-call by escorting the female hen to a nest site ŽMcBride et
al., 1969; Thornhill, 1988.. The advantage for the female of the presence of the male
probably is a better protection against predators, while the male might benefit by the
chance to copulate with the female on the way back to the group ŽMcBride et al., 1969;
Thornhill, 1988.. However, the occurrence of the gakel-call is not restricted to the
prelaying context ŽBaumer,
1962; Schenk et al., 1983; Meijsser and Hughes, 1989;
¨
Zimmerman and Koene, 1998a.. The second aim of the present study was to investigate
whether frustration in different contexts Žfood, water, dust and nest. results in a higher
number of gakel-calls. For this purpose, hens were thwarted in their feeding, drinking,
dustbathing and nesting behaviour in a situation in which they previously had access to
these commodities. Furthermore, we examined whether the various contexts of thwarting
affected temporal characteristics of the gakel-call in different ways. Schenk et al. Ž1983.
found some indication that an increasing deprivation of dustbath resulted in a higher
number of gakel-calls given in response to the thwarting of dustbathing behaviour. He
found that these gakel-calls also tended to be longer in duration and consisted of fewer
notes. So, an increase in the motivation level may be reflected in temporal characteristics of the gakel-call.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
257
We formulated the following research questions: Does frustration give rise to a higher
number of gakel-calls than the mere thwarting of behaviour? Is a state of frustration, in
general, caused by the omission of reward in different contexts Žfeeding, drinking,
dustbathing and nesting., expressed through the gakel-call and other behaviours indicative of frustration? Are there any differences between the contexts of frustration in the
number and temporal characteristics of gakel-calls?
2. Materials and methods
2.1. Animals and housing
Twenty laying hens, 10 ISA Brown and 10 ISA White Leghorns, of 23 weeks old
were housed individually in cages Ž139 = 50 = 50 cm; L = W = H .. The cages were
positioned in a row, approximately 15 cm apart. The front and top side of a cage were
made of wire-netting and the sides adjacent to the other cages contained a small
wire-netting window Ž20 = 20 cm.. Hens could have visual and auditory contact with
other hens, and the side windows allowed neighbouring hens to have tactile contact.
Each cage contained a nest Ž39 = 50 = 40 cm. and dust area Ž50 = 50 cm.. Food
Žcommercial pellets. and water were freely available outside experimental treatments.
The light period fell between 2:00 AM and 18:00 PM.
2.2. Experimental procedure
The 20 hens were subdivided in four groups containing either three ISA Brown hens
and two White Leghorns or the reverse. All groups received four treatments: they were
successively thwarted in their feeding ŽFood., drinking ŽWater., dustbathing ŽDust. and
nesting ŽNest. behaviour in a randomised way, to prevent an effect of order of
treatments. The procedure for training and testing in the treatments Food, Water and
Dust was as follows. The hens were deprived of food or water for 23 h prior to training
and testing by closing the feeder or drinker. Twenty-three hours of food deprivation had
appeared to be sufficient to elicit an increase in gakel-calls and other behaviours
indicative of frustration ŽZimmerman and Koene, 1998a,b.. We figured that 23-h dust
deprivation would not be sufficient, because hens normally take a dustbath every 2 days
ŽVestergaard, 1982.. Therefore, the dust area was covered up with a wooden lid for 72
h. After deprivation, the hens were trained to get access to food, water or dust at a fixed
time on 4 consecutive days. For this purpose, the feeder and drinker were opened for 45
min. The entrance of the experimenter and the marked removal of the cover of feeder,
drinker and dustbath served as conditioned stimuli. Because a dustbathing cycle under
unrestricted circumstances typically lasts about 30 min ŽVestergaard, 1982., the hens
were accustomed to receive 15-min access to the dust area during training. Fifteen
minutes access to dust was short enough to maintain the need to perform dustbathing
behaviour on the consecutive training and test days. After 4 days of training, a test day
258
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
followed. A test session in all treatments lasted 45 min and was subdivided in three
15-min periods:
Pre-Frustration: This period started 15 min before the time the hen was used to get
access to one of the commodities on a training day;
Frustration: At the start of this 15-min period, feeder, drinker or dust area were
opened and immediately closed again;
Post-frustration: Feeder, drinker and dust area were opened.
Training and testing in these treatments were carried out from 1200 h onwards after all
hens had laid their eggs.
The procedure of training and testing in treatment Nest was different from the other
treatments. Egg-laying occurs in a 25-h cycle and 1–2 h before egg-laying hens typically
are engaged in prelaying or nesting behaviour. The hen performs a number of nest
inspections before it finally settles on the nest ŽMcBride et al., 1969; Wood-Gush and
Gilbert, 1969.. Because it is impossible to predict the precise time of nesting behaviour,
it was impracticable to train hens to have access to the nest at a certain time and then
block this access during testing. This was the reason we thwarted the last stage of
prelaying behaviour in which the hen finally settles on the nest. For this purpose, the
hens of a group were scanned on 2 consecutive days, every 30 min from the onset of the
light period, to determine the approximate time of oviposition. On the third day, a hen
that had entered a nest was observed for 15 min ŽPre-Frustration. and after that, pushed
off the nest and the nest box was closed for 15 min ŽFrustration.. After 15 min, the nest
was opened again ŽPost-frustration..
The durations of deprivation used in the different treatments were chosen arbitrarily,
but we expected that they would motivate the animals sufficiently to try to perform the
behaviour when being thwarted. So, although we were not able to precisely assess the
intensity of thwarting in the different treatments, we assumed that the intensities would
not differ too much.
During the three experimental periods, the number of gakel-calls and alarm-cackles
were recorded. Furthermore, the durations of stereotyped pacing ŽDuncan and WoodGush, 1972b., displacement preening ŽDuncan and Wood-Gush, 1972a. and number of
escape attempts were recorded. We defined an escape attempt as the hen sticking its
head out the front of the cage, through the wire, while moving its body backwards and
forwards.
Gakel-calls were digitised using Signal w software. From gakel-calls that were not
disturbed by background noises, the mean duration, the mean number of notes and the
mean duration of the first note were determined.
2.3. Statistical analysis
We used a repeated measures analysis in the GLM-procedure in the SAS w statistical
program ŽSAS Institute, 1989. with strain, group and treatment as factors. Whenever a
significant effect of one of the factors was found, a post hoc test ŽLSMEANS. was
carried out to find the statistical differences between the levels of a factor.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
259
The effect of strain, group and treatment on mean duration and number of notes per
gakel-call were determined in a repeated measures analysis in SAS.
3. Results
No effect of strain or group on any of the behaviours recorded was found.
In treatment Food, the number of gakel-calls in period Frustration was not significantly higher than in period Pre-Frustration ŽANOVA: F1,17 s 2.60, P s 0.13; Fig. 1..
There were also no significant differences in the number of cackles ŽMean " S.E.M.:
Pre-Frustration: 0.1 " 0.1 vs. Frustration: 1.0 " 0.5. and escape attempts ŽPre-Frustration: 9.6 " 2.4 vs. Frustration: 11.6 " 3.9. between the periods Frustration and Pre-Frustration in treatment Food. In the period Frustration, the time spent in stereotyped pacing
was significantly less than in period Pre-Frustration ŽPre-Frustration: 299 " 42.4 vs.
Frustration: 240 " 41.1; ANOVA: F1,17 s 13.46, P - 0.01.. We found no significant
difference in the duration of displacement preening between the periods Pre-Frustration
and Frustration ŽPre-Frustration: 15.6 " 14.5 vs. Frustration: 44.8 " 12.3..
In treatment Water, the hens gave significantly more gakel-calls in period Frustration
than in period Pre-Frustration ŽANOVA: F1,17 s 4.90, P - 0.05; Fig. 1.. We found no
significant differences between periods Pre-Frustration and Frustration in the number of
cackles ŽPre-Frustration: 0.8 " 0.4 vs. Frustration: 0.6 " 0.5., escape attempts ŽPre-Frustration: 11.3 " 3.1 vs. Frustration: 8.8 " 2.2. and the duration of pacing ŽPre-Frustration:
285 " 39.7 vs. Frustration: 300 " 46.3. and preening ŽPre-Frustration: 16.8 " 6.4 vs.
Frustration: 7.3 " 2.2..
Fig. 1. The mean number of gakel-calls in the three experimental periods in all treatments. Signs indicate the
level of significance of the difference between periods Pre-Frustration and Frustration; N.S.: nonsignificant,
)
P - 0.05, ) ) ) P - 0.001.
260
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
Table 1
The mean number of alarm-cackles, escape attempts and the mean duration of stereotyped pacing and
displacement preening in all the treatments in period Frustration
Food
No. of alarm-cackles
No. of escape attempts
Duration of pacing Žs.
Duration of displacement preening Žs.
Water
a,b
1.0"0.5
11.6"3.9 b
240"41a
44.8"12.3 a
Dust
a,b
0.6"0.5
8.8"2.2 a
300"46 a
7.3"2.2 a
Nest
b
0.3"0.1
1.1"0.3 a
104"11b
16.1"6.0 a
8.0"3.2 a
11.4"2.5 b
306"32 a
29.8"7.4 a
Different letters indicate differences between the treatments.
In treatment Dust, hens gave significantly more gakel-calls in period Frustration than
in period Pre-Frustration ŽANOVA: F1,17 s 5.18, P - 0.05; Fig. 1.. They spent significantly less time pacing in period Frustration than in period Pre-Frustration ŽPre-Frustration: 157 " 25.2 vs. Frustration: 104 " 11.2; ANOVA: F1,17 s 5.86, P - 0.05.. No
significant differences were found in the number of cackles ŽPre-Frustration: 0.6 " 0.3
vs. Frustration: 0.3 " 0.1., escape attempts ŽPre-Frustration: 2.9 " 1.1 vs. Frustration:
1.1 " 0.3. and the duration of displacement preening ŽPre-Frustration: 8.8 " 3.6 vs.
Frustration: 16.1 " 6.0..
In treatment Nest, the hens gave significantly more gakel-calls in period Frustration
than in period Pre-Frustration ŽANOVA: F1,17 s 30.83, P - 0.001; Fig. 1.. Also, the
hens gave significantly more cackles ŽPre-Frustration: 0.0 " 0 vs. Frustration: 8.0 " 3.2;
ANOVA: F1,17 s 6.07, P - 0.05. and performed more escape attempts ŽPre-Frustration:
0.0 " 0 vs. Frustration: 11.4 " 2.5; ANOVA: F1,17 s 22.03, P - 0.001. in the period
Frustration than in the period Pre-Frustration. Furthermore, more time was spent in
pacing ŽANOVA: F1,17 s 84.79, P - 0.001. and displacement preening ŽANOVA:
F1,17 s 13.25, P - 0.01. in period Frustration Žduration of pacing: 306 " 32.7; duration
of preening: 29.8 " 7.4. than in period Pre-Frustration Žpacing: 0.0 " 0; preening:
1.8 " 1.6..
The number of gakel-calls given in period Frustration was significantly higher in
treatment Nest than in the other three treatments ŽANOVA: F1,17 s 15.84, P - 0.001..
The number of gakel-calls in period Frustration did not differ between treatments Food,
Water and Dust ŽFig. 1.. The number of alarm-cackles given in period Frustration was
significantly higher in treatment Nest than in treatment Dust ŽANOVA: F1,17 s 3.80,
P - 0.05; Table 1.. Significantly, more escape attempts were performed in period
Frustration in the treatments Food and Nest than in treatment Dust ŽANOVA: F1,17 s
4.10, P - 0.05; Table 1.. The time the hens spent pacing in period Frustration was
significantly lower in treatment Dust than in the other three treatments ŽANOVA:
F1,17 s 16.79, P - 0.001; Table 1.. The duration of displacement preening in period
Frustration did not differ between treatments ŽTable 1..
Fig. 2. The mean duration per gakel-call ŽA., the mean number of notes per gakel-call ŽB. and the mean
duration of the first note ŽC. in all treatments. Different letters or combinations of letters indicate significant
statistical differences between treatments below the 0.05 level for both the mean length and number of notes.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
261
262
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
We found a significant effect of treatment on both the mean length per gakel-call
ŽANOVA: F1,16 s 6.41, P - 0.001; Fig. 2A. and the mean number of notes per
gakel-call ŽANOVA: F1,16 s 13.84, P - 0.001; Fig. 2B. in period Frustration. Both
mean length and number of notes per gakel-call were significantly higher in treatment
Nest than in treatments Water and Dust. No effect of treatment was found on the length
of the first note ŽFig. 2C..
No significant positive correlation ŽSpearman rank correlation. between mean length
and number of notes per gakel-call was found in any of the treatments. A significant
positive correlation between the length of the first note and the total length per
gakel-call was found in treatment Dust Ž r s 0.78, P - 0.05.. This tended to be the case
in treatment Water Ž r s 0.67, P s 0.9..
4. Discussion
The present study shows that deprivation plus additional frustration in a water and
dustbath context is reflected in a higher number of gakel-calls compared to deprivation
alone. We did not find such an increase in the number of gakel-calls in the food context,
unlike very clear results in previous studies ŽZimmerman and Koene, 1998a,b.. An
explanation for the major difference between the previous and the present study might
be the procedure of frustration. In our previous experiments, hens were thwarted in their
feeding behaviour in a conditioning paradigm. In a control session, every 30 s hens were
rewarded with 5-s access to food after the conditioned stimulus or operant response. In a
15-min frustration session, the food reward was omitted by presenting the hens an empty
feeder. Such a session typically consisted of approximately 23 trials in which the hens
were presented the empty feeder in every trial. The state of frustration elicited in the
frustration session in the previous experiment might have been more intense than in the
period Frustration in the present study. The difference in mean number of gakel-calls in
both 15-min periods of frustration in the food context Žpresent study: 6.9, previous
study: 22. might be a reflection of the difference in the degree of frustration between the
experiments. Furthermore, in the present study, the comparison was made between
deprivation and frustration treatment; while in the previous study, a frustration session
was compared to a control session. This difference in type of comparison also might
have accounted for the nonsignificant difference in the number of gakel-calls between
frustration and its ‘‘control’’, in contrast to previous findings.
In the period Frustration, the number of gakel-calls was higher in treatment Nest than
in the other treatments. This might mean that in this treatment the level of frustration
was higher. However, this is not supported by higher levels of other behaviours
indicative of frustration in treatment Nest compared to the other treatments. An
alternative explanation for the higher number of gakel-calls in treatment Nest is
suggested by the occurrence of the gakel-call under natural circumstances. The gakel-call
is given before oviposition and probably has evolved as a signal towards the rooster
ŽMcBride et al., 1969; Thornhill, 1988.. According to Meijsser and Hughes Ž1989., the
performance of the gakel-call is related to finding a suitable nest site, also under
husbandry conditions. Another explanation is offered by the motivational model
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
263
proposed by Wiepkema Ž1987.. It implies that the gakel-call under these circumstances
is an emotional expression of the detection of a prolonged mismatch between actual
Ž‘‘no nest site found’’. state and desired state Ž‘‘find a suitable nest site’’. and is an
indication of frustration. Both oviposition and the detection of a prolonged mismatch
could at the same time contribute to the occurrence of gakel-calls. The surplus of
gakel-calls in treatment Nest compared to the other treatments might be the gakel-calls
specifically related to oviposition.
This latter finding might account for the difference in temporal characteristics of
gakel-calls between treatment Nest and the treatments Water and Dust. Gakel-calls in
treatment Nest lasted longer and consisted of more notes than in the treatments Water
and Dust. Schenk et al. Ž1983. found that the mean duration of a single gakel-call was
longer when dustbathing was thwarted stronger by longer deprivation. However, from
the present study, nothing decisive can be concluded about the relation between the
number of gakel-calls and their temporal characteristics on the one hand, and the
intensity of thwarting in the different treatments on the other.
5. Conclusions
In conclusion, the results from the present and previous studies suggest that both
deprivation and the additional frustration, in general, in laying hens is expressed through
the gakel-call. The higher number of gakel-calls in the nest context merits further
research into the functional aspects of this frustration call.
References
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alternative systems. Br. Poult. Sci. 30, 747–760.
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www.elsevier.comrlocaterapplanim
Thwarting of behaviour in different contexts and the
gakel-call in the laying hen
Patrick H. Zimmerman a,) , Paul Koene a , Jan A.R.A.M. van Hooff
a
b
Ethology Group, Wageningen Agricultural UniÕersity, P.O. Box 338, 6700 AH Wageningen, Netherlands
b
Project Group Ethology and Socio-Ecology, P.O. Box 80086, 3508 TB Utrecht, Netherlands
Accepted 14 April 2000
Abstract
Earlier studies have shown that thwarting of feeding behaviour in the laying hen is expressed
through a specific vocalisation, the gakel-call. The first aim of this study was to investigate
whether the effect of deprivation per se on the occurrence of gakel-calls can be distinguished from
the effect of the additional frustration. Frustration is defined as the state of an animal that results
from nonreward in the expectancy of reward. The second aim was to investigate whether the
occurrence of gakel-calls is restricted to a food context or whether it can be regarded as an
expression of frustration in general. For this purpose, 20 hens were deprived of food, water and
dustbath. After deprivation at a fixed time, a cue was given and the hens were rewarded with
access to food, water or dust during a 15-min session on 4 consecutive days. On the fifth day, they
were thwarted in the associated behaviours by blocking the access to these commodities, after the
hens had been presented the signal that previously preceded the reward. We then recorded
behaviours that might reflect the state of frustration in three 15-min periods. The period
‘‘Pre-Frustration’’ started 15 min before ‘‘Frustration’’. This, in turn, was followed by the period
‘‘Post-frustration’’ in which the hens were rewarded again. Nesting behaviour was thwarted by
blocking the access to the nest ŽFrustration. after a hen had reached the last stage of its prelaying
behaviour.
In the food, water and dustbath context, deprivation elicited gakel-calls. The additional
frustration resulted in a higher number of gakel-calls in all contexts except the food context.
However, together with the findings of previous experiments, the results of this study suggest that
frustration, in general, is expressed through the gakel-call. Frustration in the nest context elicited
more gakel-calls than the other contexts. This latter finding is discussed in the light of the
)
Corresponding author. Tel.: q31-317-483926; fax: q31-317-485006.
E-mail address: patrick.zimmerman@etho.vh.wau.nl ŽP.H. Zimmerman..
0168-1591r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 1 5 9 1 Ž 0 0 . 0 0 1 3 7 - 4
256
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
occurrence of the gakel-call under natural circumstances. q 2000 Elsevier Science B.V. All rights
reserved.
Keywords: Chicken welfare; Frustration; Deprivation; Vocalisation; Feeding; Drinking; Dustbathing; Prelaying
1. Introduction
In domestic laying hens, an increase in behaviours such as stereotyped pacing,
displacement preening and the occurrence of a specific vocalisation, the gakel-call, is
associated with thwarting of feeding ŽDuncan and Wood-Gush, 1972a,b; Schenk et al.,
1983; Zimmerman and Koene, 1998a., dustbathing ŽKoene and Wiepkema, 1991. and
nesting behaviour Že.g. Schenk et al., 1983; Meijsser and Hughes, 1989; Freire et al.,
1996.. Thwarting a behaviour that ensures fulfillment of ethological needs impairs
welfare. Animal welfare is the state of the animal regarding its attempt to fulfill its needs
ŽBroom, 1996.. A number of studies suggests that the gakel-call is given in reaction to
the thwarting of behaviour ŽSchenk et al., 1983; Meijsser and Hughes, 1989; Koene and
Wiepkema, 1991; Zimmerman and Koene, 1998a.. Behaviours, which are given in
response to the thwarting of behaviour, can be used as indicators of the subsequent state
of frustration and may, therefore, qualify as measures of welfare ŽDawkins, 1990;
Duncan, 1992.. Frustration has been defined as ‘‘an aversive motivational state that
results from nonreward, reduced reward or delayed reward in the presence of a history
of reward’’ ŽAmsel, 1992.. From this definition, it follows that the effect of mere
thwarting of behaviour might be distinguishable from the effect of frustration. The first
aim of the present study was to investigate whether the effect of deprivation on the
occurrence of gakel-calls could be distinguished from the effect of the additional
frustration.
Under natural conditions, it has been described that a female hen, which is about to
leave the group to find a suitable nest site, utters the gakel-call. As a rule, the dominant
male responds to the gakel-call by escorting the female hen to a nest site ŽMcBride et
al., 1969; Thornhill, 1988.. The advantage for the female of the presence of the male
probably is a better protection against predators, while the male might benefit by the
chance to copulate with the female on the way back to the group ŽMcBride et al., 1969;
Thornhill, 1988.. However, the occurrence of the gakel-call is not restricted to the
prelaying context ŽBaumer,
1962; Schenk et al., 1983; Meijsser and Hughes, 1989;
¨
Zimmerman and Koene, 1998a.. The second aim of the present study was to investigate
whether frustration in different contexts Žfood, water, dust and nest. results in a higher
number of gakel-calls. For this purpose, hens were thwarted in their feeding, drinking,
dustbathing and nesting behaviour in a situation in which they previously had access to
these commodities. Furthermore, we examined whether the various contexts of thwarting
affected temporal characteristics of the gakel-call in different ways. Schenk et al. Ž1983.
found some indication that an increasing deprivation of dustbath resulted in a higher
number of gakel-calls given in response to the thwarting of dustbathing behaviour. He
found that these gakel-calls also tended to be longer in duration and consisted of fewer
notes. So, an increase in the motivation level may be reflected in temporal characteristics of the gakel-call.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
257
We formulated the following research questions: Does frustration give rise to a higher
number of gakel-calls than the mere thwarting of behaviour? Is a state of frustration, in
general, caused by the omission of reward in different contexts Žfeeding, drinking,
dustbathing and nesting., expressed through the gakel-call and other behaviours indicative of frustration? Are there any differences between the contexts of frustration in the
number and temporal characteristics of gakel-calls?
2. Materials and methods
2.1. Animals and housing
Twenty laying hens, 10 ISA Brown and 10 ISA White Leghorns, of 23 weeks old
were housed individually in cages Ž139 = 50 = 50 cm; L = W = H .. The cages were
positioned in a row, approximately 15 cm apart. The front and top side of a cage were
made of wire-netting and the sides adjacent to the other cages contained a small
wire-netting window Ž20 = 20 cm.. Hens could have visual and auditory contact with
other hens, and the side windows allowed neighbouring hens to have tactile contact.
Each cage contained a nest Ž39 = 50 = 40 cm. and dust area Ž50 = 50 cm.. Food
Žcommercial pellets. and water were freely available outside experimental treatments.
The light period fell between 2:00 AM and 18:00 PM.
2.2. Experimental procedure
The 20 hens were subdivided in four groups containing either three ISA Brown hens
and two White Leghorns or the reverse. All groups received four treatments: they were
successively thwarted in their feeding ŽFood., drinking ŽWater., dustbathing ŽDust. and
nesting ŽNest. behaviour in a randomised way, to prevent an effect of order of
treatments. The procedure for training and testing in the treatments Food, Water and
Dust was as follows. The hens were deprived of food or water for 23 h prior to training
and testing by closing the feeder or drinker. Twenty-three hours of food deprivation had
appeared to be sufficient to elicit an increase in gakel-calls and other behaviours
indicative of frustration ŽZimmerman and Koene, 1998a,b.. We figured that 23-h dust
deprivation would not be sufficient, because hens normally take a dustbath every 2 days
ŽVestergaard, 1982.. Therefore, the dust area was covered up with a wooden lid for 72
h. After deprivation, the hens were trained to get access to food, water or dust at a fixed
time on 4 consecutive days. For this purpose, the feeder and drinker were opened for 45
min. The entrance of the experimenter and the marked removal of the cover of feeder,
drinker and dustbath served as conditioned stimuli. Because a dustbathing cycle under
unrestricted circumstances typically lasts about 30 min ŽVestergaard, 1982., the hens
were accustomed to receive 15-min access to the dust area during training. Fifteen
minutes access to dust was short enough to maintain the need to perform dustbathing
behaviour on the consecutive training and test days. After 4 days of training, a test day
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P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
followed. A test session in all treatments lasted 45 min and was subdivided in three
15-min periods:
Pre-Frustration: This period started 15 min before the time the hen was used to get
access to one of the commodities on a training day;
Frustration: At the start of this 15-min period, feeder, drinker or dust area were
opened and immediately closed again;
Post-frustration: Feeder, drinker and dust area were opened.
Training and testing in these treatments were carried out from 1200 h onwards after all
hens had laid their eggs.
The procedure of training and testing in treatment Nest was different from the other
treatments. Egg-laying occurs in a 25-h cycle and 1–2 h before egg-laying hens typically
are engaged in prelaying or nesting behaviour. The hen performs a number of nest
inspections before it finally settles on the nest ŽMcBride et al., 1969; Wood-Gush and
Gilbert, 1969.. Because it is impossible to predict the precise time of nesting behaviour,
it was impracticable to train hens to have access to the nest at a certain time and then
block this access during testing. This was the reason we thwarted the last stage of
prelaying behaviour in which the hen finally settles on the nest. For this purpose, the
hens of a group were scanned on 2 consecutive days, every 30 min from the onset of the
light period, to determine the approximate time of oviposition. On the third day, a hen
that had entered a nest was observed for 15 min ŽPre-Frustration. and after that, pushed
off the nest and the nest box was closed for 15 min ŽFrustration.. After 15 min, the nest
was opened again ŽPost-frustration..
The durations of deprivation used in the different treatments were chosen arbitrarily,
but we expected that they would motivate the animals sufficiently to try to perform the
behaviour when being thwarted. So, although we were not able to precisely assess the
intensity of thwarting in the different treatments, we assumed that the intensities would
not differ too much.
During the three experimental periods, the number of gakel-calls and alarm-cackles
were recorded. Furthermore, the durations of stereotyped pacing ŽDuncan and WoodGush, 1972b., displacement preening ŽDuncan and Wood-Gush, 1972a. and number of
escape attempts were recorded. We defined an escape attempt as the hen sticking its
head out the front of the cage, through the wire, while moving its body backwards and
forwards.
Gakel-calls were digitised using Signal w software. From gakel-calls that were not
disturbed by background noises, the mean duration, the mean number of notes and the
mean duration of the first note were determined.
2.3. Statistical analysis
We used a repeated measures analysis in the GLM-procedure in the SAS w statistical
program ŽSAS Institute, 1989. with strain, group and treatment as factors. Whenever a
significant effect of one of the factors was found, a post hoc test ŽLSMEANS. was
carried out to find the statistical differences between the levels of a factor.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
259
The effect of strain, group and treatment on mean duration and number of notes per
gakel-call were determined in a repeated measures analysis in SAS.
3. Results
No effect of strain or group on any of the behaviours recorded was found.
In treatment Food, the number of gakel-calls in period Frustration was not significantly higher than in period Pre-Frustration ŽANOVA: F1,17 s 2.60, P s 0.13; Fig. 1..
There were also no significant differences in the number of cackles ŽMean " S.E.M.:
Pre-Frustration: 0.1 " 0.1 vs. Frustration: 1.0 " 0.5. and escape attempts ŽPre-Frustration: 9.6 " 2.4 vs. Frustration: 11.6 " 3.9. between the periods Frustration and Pre-Frustration in treatment Food. In the period Frustration, the time spent in stereotyped pacing
was significantly less than in period Pre-Frustration ŽPre-Frustration: 299 " 42.4 vs.
Frustration: 240 " 41.1; ANOVA: F1,17 s 13.46, P - 0.01.. We found no significant
difference in the duration of displacement preening between the periods Pre-Frustration
and Frustration ŽPre-Frustration: 15.6 " 14.5 vs. Frustration: 44.8 " 12.3..
In treatment Water, the hens gave significantly more gakel-calls in period Frustration
than in period Pre-Frustration ŽANOVA: F1,17 s 4.90, P - 0.05; Fig. 1.. We found no
significant differences between periods Pre-Frustration and Frustration in the number of
cackles ŽPre-Frustration: 0.8 " 0.4 vs. Frustration: 0.6 " 0.5., escape attempts ŽPre-Frustration: 11.3 " 3.1 vs. Frustration: 8.8 " 2.2. and the duration of pacing ŽPre-Frustration:
285 " 39.7 vs. Frustration: 300 " 46.3. and preening ŽPre-Frustration: 16.8 " 6.4 vs.
Frustration: 7.3 " 2.2..
Fig. 1. The mean number of gakel-calls in the three experimental periods in all treatments. Signs indicate the
level of significance of the difference between periods Pre-Frustration and Frustration; N.S.: nonsignificant,
)
P - 0.05, ) ) ) P - 0.001.
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P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
Table 1
The mean number of alarm-cackles, escape attempts and the mean duration of stereotyped pacing and
displacement preening in all the treatments in period Frustration
Food
No. of alarm-cackles
No. of escape attempts
Duration of pacing Žs.
Duration of displacement preening Žs.
Water
a,b
1.0"0.5
11.6"3.9 b
240"41a
44.8"12.3 a
Dust
a,b
0.6"0.5
8.8"2.2 a
300"46 a
7.3"2.2 a
Nest
b
0.3"0.1
1.1"0.3 a
104"11b
16.1"6.0 a
8.0"3.2 a
11.4"2.5 b
306"32 a
29.8"7.4 a
Different letters indicate differences between the treatments.
In treatment Dust, hens gave significantly more gakel-calls in period Frustration than
in period Pre-Frustration ŽANOVA: F1,17 s 5.18, P - 0.05; Fig. 1.. They spent significantly less time pacing in period Frustration than in period Pre-Frustration ŽPre-Frustration: 157 " 25.2 vs. Frustration: 104 " 11.2; ANOVA: F1,17 s 5.86, P - 0.05.. No
significant differences were found in the number of cackles ŽPre-Frustration: 0.6 " 0.3
vs. Frustration: 0.3 " 0.1., escape attempts ŽPre-Frustration: 2.9 " 1.1 vs. Frustration:
1.1 " 0.3. and the duration of displacement preening ŽPre-Frustration: 8.8 " 3.6 vs.
Frustration: 16.1 " 6.0..
In treatment Nest, the hens gave significantly more gakel-calls in period Frustration
than in period Pre-Frustration ŽANOVA: F1,17 s 30.83, P - 0.001; Fig. 1.. Also, the
hens gave significantly more cackles ŽPre-Frustration: 0.0 " 0 vs. Frustration: 8.0 " 3.2;
ANOVA: F1,17 s 6.07, P - 0.05. and performed more escape attempts ŽPre-Frustration:
0.0 " 0 vs. Frustration: 11.4 " 2.5; ANOVA: F1,17 s 22.03, P - 0.001. in the period
Frustration than in the period Pre-Frustration. Furthermore, more time was spent in
pacing ŽANOVA: F1,17 s 84.79, P - 0.001. and displacement preening ŽANOVA:
F1,17 s 13.25, P - 0.01. in period Frustration Žduration of pacing: 306 " 32.7; duration
of preening: 29.8 " 7.4. than in period Pre-Frustration Žpacing: 0.0 " 0; preening:
1.8 " 1.6..
The number of gakel-calls given in period Frustration was significantly higher in
treatment Nest than in the other three treatments ŽANOVA: F1,17 s 15.84, P - 0.001..
The number of gakel-calls in period Frustration did not differ between treatments Food,
Water and Dust ŽFig. 1.. The number of alarm-cackles given in period Frustration was
significantly higher in treatment Nest than in treatment Dust ŽANOVA: F1,17 s 3.80,
P - 0.05; Table 1.. Significantly, more escape attempts were performed in period
Frustration in the treatments Food and Nest than in treatment Dust ŽANOVA: F1,17 s
4.10, P - 0.05; Table 1.. The time the hens spent pacing in period Frustration was
significantly lower in treatment Dust than in the other three treatments ŽANOVA:
F1,17 s 16.79, P - 0.001; Table 1.. The duration of displacement preening in period
Frustration did not differ between treatments ŽTable 1..
Fig. 2. The mean duration per gakel-call ŽA., the mean number of notes per gakel-call ŽB. and the mean
duration of the first note ŽC. in all treatments. Different letters or combinations of letters indicate significant
statistical differences between treatments below the 0.05 level for both the mean length and number of notes.
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
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P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
We found a significant effect of treatment on both the mean length per gakel-call
ŽANOVA: F1,16 s 6.41, P - 0.001; Fig. 2A. and the mean number of notes per
gakel-call ŽANOVA: F1,16 s 13.84, P - 0.001; Fig. 2B. in period Frustration. Both
mean length and number of notes per gakel-call were significantly higher in treatment
Nest than in treatments Water and Dust. No effect of treatment was found on the length
of the first note ŽFig. 2C..
No significant positive correlation ŽSpearman rank correlation. between mean length
and number of notes per gakel-call was found in any of the treatments. A significant
positive correlation between the length of the first note and the total length per
gakel-call was found in treatment Dust Ž r s 0.78, P - 0.05.. This tended to be the case
in treatment Water Ž r s 0.67, P s 0.9..
4. Discussion
The present study shows that deprivation plus additional frustration in a water and
dustbath context is reflected in a higher number of gakel-calls compared to deprivation
alone. We did not find such an increase in the number of gakel-calls in the food context,
unlike very clear results in previous studies ŽZimmerman and Koene, 1998a,b.. An
explanation for the major difference between the previous and the present study might
be the procedure of frustration. In our previous experiments, hens were thwarted in their
feeding behaviour in a conditioning paradigm. In a control session, every 30 s hens were
rewarded with 5-s access to food after the conditioned stimulus or operant response. In a
15-min frustration session, the food reward was omitted by presenting the hens an empty
feeder. Such a session typically consisted of approximately 23 trials in which the hens
were presented the empty feeder in every trial. The state of frustration elicited in the
frustration session in the previous experiment might have been more intense than in the
period Frustration in the present study. The difference in mean number of gakel-calls in
both 15-min periods of frustration in the food context Žpresent study: 6.9, previous
study: 22. might be a reflection of the difference in the degree of frustration between the
experiments. Furthermore, in the present study, the comparison was made between
deprivation and frustration treatment; while in the previous study, a frustration session
was compared to a control session. This difference in type of comparison also might
have accounted for the nonsignificant difference in the number of gakel-calls between
frustration and its ‘‘control’’, in contrast to previous findings.
In the period Frustration, the number of gakel-calls was higher in treatment Nest than
in the other treatments. This might mean that in this treatment the level of frustration
was higher. However, this is not supported by higher levels of other behaviours
indicative of frustration in treatment Nest compared to the other treatments. An
alternative explanation for the higher number of gakel-calls in treatment Nest is
suggested by the occurrence of the gakel-call under natural circumstances. The gakel-call
is given before oviposition and probably has evolved as a signal towards the rooster
ŽMcBride et al., 1969; Thornhill, 1988.. According to Meijsser and Hughes Ž1989., the
performance of the gakel-call is related to finding a suitable nest site, also under
husbandry conditions. Another explanation is offered by the motivational model
P.H. Zimmerman et al.r Applied Animal BehaÕiour Science 69 (2000) 255–264
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proposed by Wiepkema Ž1987.. It implies that the gakel-call under these circumstances
is an emotional expression of the detection of a prolonged mismatch between actual
Ž‘‘no nest site found’’. state and desired state Ž‘‘find a suitable nest site’’. and is an
indication of frustration. Both oviposition and the detection of a prolonged mismatch
could at the same time contribute to the occurrence of gakel-calls. The surplus of
gakel-calls in treatment Nest compared to the other treatments might be the gakel-calls
specifically related to oviposition.
This latter finding might account for the difference in temporal characteristics of
gakel-calls between treatment Nest and the treatments Water and Dust. Gakel-calls in
treatment Nest lasted longer and consisted of more notes than in the treatments Water
and Dust. Schenk et al. Ž1983. found that the mean duration of a single gakel-call was
longer when dustbathing was thwarted stronger by longer deprivation. However, from
the present study, nothing decisive can be concluded about the relation between the
number of gakel-calls and their temporal characteristics on the one hand, and the
intensity of thwarting in the different treatments on the other.
5. Conclusions
In conclusion, the results from the present and previous studies suggest that both
deprivation and the additional frustration, in general, in laying hens is expressed through
the gakel-call. The higher number of gakel-calls in the nest context merits further
research into the functional aspects of this frustration call.
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